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Neuroscience and Biobehavioral Reviews 36 (2012) 431–438

Contents lists available at ScienceDirect

Neuroscience and Biobehavioral Reviews

jou rna l h omepa ge: www.elsev ier .com/ locate /neubiorev

eview

ognitive mechanisms of auditory verbal hallucinations in psychotic andon-psychotic groups

ohanna C. Badcocka,b,∗, Kenneth Hugdahlc,d

School of Psychiatry and Clinical Neurosciences, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, AustraliaCentre for Clinical Research in Neuropsychiatry/Graylands Hospital, Private Mail Bag No. 1, Claremont, WA 6910, AustraliaDepartment of Biological and Medical Psychology/Cognitive NeuroScience Group, University of Bergen, NorwayDivision of Psychiatry, Haukeland University Hospital, Bergen, Norway

r t i c l e i n f o

rticle history:eceived 3 May 2011eceived in revised form 7 July 2011ccepted 23 July 2011

eywords:uditory hallucinations

a b s t r a c t

The continuum model of psychosis has been extremely influential. It assumes that psychotic symptoms,such as auditory verbal hallucinations (AVH), are not limited to patients with psychosis but also occur inhealthy, non-clinical individuals – suggesting similar mechanisms of origin. Recent debate surroundingthis model has highlighted certain differences, as well as similarities, in the phenomenology of AVH inclinical and non-clinical populations. These findings imply that there may, in fact, be only partial overlapof the mechanism(s) involved in generating AVH in these groups. We review evidence of continuity or

allucination predispositionchizophreniaognition

similarity, and dissimilarity, in cognitive, and related neural processes, underlying AVH in clinical andnon-clinical samples. The results reveal some shared (intrusive cognitions, inhibitory deficits) and somedistinct (aspects of source memory and cerebral lateralization) mechanisms in these groups. The evidence,therefore, supports both continuous and categorical models of positive psychotic symptoms. The reviewconsiders potential risks of uncritical acceptance of the continuum model and highlights some importantmethodological issues for future research.

© 2011 Elsevier Ltd. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4312. Overview of findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 432

2.1. Intrusive cognitions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4322.2. Source memory and contextual integration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4332.3. Inhibitory control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4342.4. Lateralization and the cerebral hemispheres . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 434

3. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4354. Summary and main conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436

Conflict of interest statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436

. Introduction 2007; Johns and van Os, 2001; van Os et al., 2009; Verdoux and

In recent years, a dimensional approach to understandingsychotic symptoms has become firmly established, commonlyeferred to as the continuum model of psychosis (Allardyce et al.,

∗ Corresponding author at: School of Psychiatry and Clinical Neurosciences, Uni-ersity of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.el.: +61 8 9347 6507; fax: +61 8 9384 5128.

E-mail addresses: johanna.badcock@uwa.edu.au (J.C. Badcock),ugdahl@psybp.uib.no (K. Hugdahl).

149-7634/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.oi:10.1016/j.neubiorev.2011.07.010

van Os, 2002, for reviews). A wealth of empirical evidence nowshows, for example, that auditory verbal hallucinations (AVH) arecommonly reported by healthy individuals without mental ill-ness, as well as those diagnosed with a psychotic disorder, such asschizophrenia (e.g. Sommer et al., 2010). Such findings suggest thatthe experience of hearing voices lies on a continuum with normality(Claridge, 1990, for a theoretical model; Choong et al., 2007; Pierre,

2010; Stip and Letourneau, 2009, for reviews). The rate of AVHreported in the general population varies, as a result of methodolog-ical and design factors, from 5.7–21.0% in children and adolescents(e.g. Bartels-Velthuis et al., 2010; McGee et al., 2000) to 10–15% of

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he adult population (Tien, 1991; Sommer et al., 2010). The majorityf these hallucinatory experiences are transitory but some persist

increasing the risk of secondary delusional ideation and transi-ion to psychosis (see De Loore et al., 2011; Dominguez et al., 2011;meets et al., 2010, for empirical evidence; van Os et al., 2009, for

review). Interestingly, Bartels-Velthuis et al. (2011) found bet-er theory-of-mind skills in children hearing voices, a finding theuthors suggested could mitigate the risk of secondary delusionormation.

The presence of a continuum of psychotic symptoms is oftenaken to imply fundamentally the same phenomenological expe-ience which, though varying in severity depends upon the sameognitive and neural mechanisms in psychotic and non-psychoticopulations (see Esterberg and Compton, 2009 as an example).onsequently, it is commonly stated that studying hallucinatoryxperiences in non-clinical samples is likely to unveil the essen-ial cognitive and neural mechanisms underlying schizophrenicallucinations, while avoiding confounding effects associated withedication, hospitalization and illness duration. The advantages

ssociated with the continuum model have led some to call for aimensional approach to the classification of psychotic disordersDutta et al., 2007; Peralta and Cuesta, 2007, for reviews and discus-ions). Nonetheless, several authors have called for a re-evaluationf the continuum concept (see discussion by David, 2010; andelated commentaries by Kaymaz and van Os, 2010; Sommer, 2010)herein AVH are assumed to be not inherently pathological, and

et at the core of psychosis.One important and potentially revealing challenge to the

ontinuum model emerges from phenomenological comparisonsetween clinical (psychotic) and non-clinical (healthy) AVH.lthough these point to some similarities in the characteristic fea-

ures of AVH in both groups (voices heard inside or outside theead, loudness, number of voices, and attribution of voices to aeal or familiar person) and a continuum of disability, they alsoighlight significant differences, as first reported by Honig et al.1998) and Romme and Escher (1989). In particular, recent datarovided in separate studies by Daalman et al. (2011) and Lawrencet al. (2010) show that a cluster of features – the frequency, emo-ional valence of beliefs and content, experience of control, age ofnset and preponderance of male voices – clearly distinguishes AVHeard by patients with schizophrenia from those experienced byealthy (non-psychotic) adults in the general community. Thesendings raise the possibility that there may be only partial over-

ap in AVH experiences and the underlying cognitive (and neural)echanisms involved (Kaymaz and van Os, 2010), in these groups.oreover, current cognitive models of AVH assume that more than

ne mechanism is likely to be involved in the development of hal-ucinations (see discussions and literature overviews by Hugdahl,009; Jones, 2008; Seal et al., 2004; Waters et al., 2006a). Such mod-ls also leave scope for the possibility that only some, but not all,ognitive mechanisms underpinning AVH occur on a continuum.

The aim of this paper, therefore, was to review current evidenceegarding similarities and dissimilarities in cognitive processesnderlying AVH in psychosis and in healthy, non-clinical popula-ions.

. Overview of findings

We conducted a selective, theoretically guided review ratherhan a formal meta-analysis of the literature, focusing on fournfluential cognitive models of AVH in patients with schizophrenia

intrusive cognitions, source memory, inhibition and lateraliza-ion) followed by a search for comparable evidence in non-clinicalamples. Within each of these four domains, all cognitive meth-ds/paradigms were considered eligible for inclusion. The review

behavioral Reviews 36 (2012) 431–438

also incorporated information regarding underling neural pro-cesses and networks relevant to each cognitive deficit. Otherimportant and well supported cognitive models of AVH have beenproposed, but were not included in this review. In particular theInner Speech/Self Monitoring Model (Bentall, 1990) has been exten-sively studied but has recently been reviewed elsewhere (Asai et al.,2009; Waters et al., 2010). Literature searches began with Med-line and Psycinfo, using relevant search terms, and then searchingthe associated reference lists and citation listings. The scope of thereview was limited to papers published in English. For the sakeof clarity, the references cited represent empirical studies, unlessotherwise indicated.

2.1. Intrusive cognitions

By definition, AVH occur in the absence of a triggering, exter-nal sensory stimulus; consequently, they must arise as a result ofdysfunctional activation of corresponding internal auditory repre-sentations (e.g. see discussion by Badcock, 2010). Current opinion isstill divided over the question of whether hallucinatory experiencesare an outcome of relatively autonomous or planned activation ofcore cognitive (e.g. perception and memory) and neural mecha-nisms (reviewed by Allen et al., 2008). However, all existing modelsof AVH assume that dysfunctional activation intrudes into ongoingneural and cognitive processing (Hugdahl et al., 2009; see Jones,2008, for a critique of current models). Such a basis is in keepingwith the ‘unbidden, intrusive character’ of the experience (Nayaniand David, 1996) which patients find particularly helpful to distin-guish hallucinated voices from ordinary verbal thought (Hoffmanet al., 2008b). Aside from the conceptual similarity to intrusive cog-nitions, cognitive accounts of AVH differ in their explanation ofthe content (i.e. what) – namely thoughts, images or memories –and the processes (i.e. how) associated with intrusive cognitions inclinical and non-clinical populations.

One influential line of empirical studies and subsequent modelsdeveloped by Morrison and colleagues, for example, has concep-tualized both clinical and non-clinical AVH as a variant of normal,intrusive thoughts: all comprise unwanted, uncontrollable cogni-tions with similar themes and content that typically interruptsongoing activity (see Morrison, 2001, 2005, for summaries of thisline of work). In contrast, the authors propose that it is the process ofappraising, interpreting and responding to intrusive thoughts thatdistinguishes psychotic from non-psychotic hallucinations. Theassessment of intrusive thoughts relies largely on self-report viaquestionnaires which have shown that the frequency of intrusivethoughts is higher in schizophrenia patients with AVH compared topsychiatric or healthy controls (Morrison and Baker, 2000). Impor-tantly, subsequent empirical studies have confirmed that healthyindividuals predisposed to hallucinations also report more intru-sive thoughts than those with low levels of hallucination proneness(Jones and Fernyhough, 2006). Statistical modelling of a vari-ety of self-report measures also indicates that intrusive thoughtscontribute significantly to hallucination predisposition (Jones andFernyhough, 2009). While such findings appear to be compatiblewith Morrison’s model – in which intrusive thoughts are cast asthe ‘raw material’ for AVH – recent phenomenological evidenceshows that clinical and non-clinical AVH differ significantly in emo-tional content, although not with regard to the perceived location(inside/outside of the head) or subjective reality (Daalman et al.,2011). A modified account, therefore, might be that clinical andnon-clinical AVH have a common basis in frequent cognitive intru-sions (grounded in neural over-activation) but differ in the content

and thus the subsequent interpretation of, or response to, thoseintrusions.

A second line of studies links AVH with intrusive auditoryimagery. Mental images are similar to hallucinatory experiences

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n that both invoke perceptual experiences in the absence of cor-esponding external stimulation (Sack et al., 2005) but are usuallyonsidered to be under at least some degree of voluntary control.either abnormally vivid nor abnormally reduced auditory imagery

s consistently associated with the presence of AVH in clinical oron-clinical populations (see literature search and reviews by Sealt al., 2004; Hubbard, 2010). Furthermore, the correlation betweenelf-reported imagery vividness and the tendency to hallucina-ions is very low, suggesting they are functionally independentSack et al., 2005; Oertel et al., 2009). The available evidence,herefore, undermines a direct, mechanistic (causal) link betweenmagery vividness and AVH. Nonetheless, auditory imagery andVH are associated with overlapping neural networks in psychotic

reviewed in Allen et al., 2008) and in non-psychotic individu-ls (Linden et al., 2011), most notably including activation of theuman voice area. This similar activation of brain regions sensi-ive to human voices indicates a common, central mechanism forVH in clinical and non-clinical samples that may explain whyallucinated voices in both groups are typically attributed to realr familiar people (Daalman et al., 2011). It should be pointedut, though, that conclusions from the Linden et al.’s (2011) studyhould be drawn with caution because of the small sample sizen = 7). How such activation arises in the absence of external stim-lation is still unclear, though several explanations have beenroposed. For example, Hunter et al. (2006) used functional mag-etic resonance imaging (fMRI) and found that normal variation

n the propensity for spontaneous activation in speech-sensitiveuditory cortex – could provide the substrate for AVH in the gen-ral population. Similar conclusions were reported by Ford et al.2009) who showed that patients with AVH were tonically “tunedn” to internal auditory representations, and Rotarska-Jagiela et al.2010), who also found differences in the level of activity in theesting-state network between patients and healthy controls. Inontrast, others have proposed that in psychosis pathology else-here in the temporal cortex could drive the activation, before

preading through fronto-temporal language networks (Shergillt al., 2004; Hoffman et al., 2008a). Importantly, functional imag-ng data in non-clinical hallucinators does not support such a modelLinden et al., 2011), consequently the current evidence leaves openhe possibility that the source of intrusive voices is different inlinical and non-clinical AVH.

A third approach has emphasized the role of intrusive mem-ries, rather than thoughts or imagery, in AVH (see Hoffman,986; Hemsley, 1993, for reviews and discussions). For exam-le, Hemsley (1993) argued that AVH arise from intrusions ofnexpected or unintended material from long-term memory.emory-based models of AVH have often been criticized as being

henomenological consistent with only a limited subset of hal-ucinatory experiences (see Jones, 2008, for an overview andiscussion). Nonetheless, abnormal structure and functioning inhe medial temporal lobe (MTL) – the region most closely involvedn episodic memory – has been consistently associated with AVHn schizophrenia (Behrendt, 2010, for a review; Jardri et al., 2011,or meta-analysis; Zierhut et al., 2010, for providing fMRI data).t is important, however, to be aware that while the Behrendt’s2010) paper was a theoretical review, the Jardri et al.’s (2011)aper was a meta-analysis. Despite this difference it is neverthe-

ess interesting that both studies come up with essentially the sameonclusion. These studies suggest that neural mechanisms involvedn episodic memory may trigger, or increase the vulnerability to,

broad (rather than narrow) array of hallucinatory experiences.onsistent with this view, cognitive studies have also shown that

ntrusive memories are associated with both clinical and non-linical hallucinations (Brébion et al., 2005, 1998; Moritz et al.,001). For example, the most commonly used method has been toeasure the number of extra-list word errors in verbal free recall

behavioral Reviews 36 (2012) 431–438 433

in individuals with, or without a predisposition to AVH. Resultsof these studies have shown a higher rate of intrusion of extra-listwords, unrelated to recall efficiency, in patients with schizophrenia(Brébion et al., 2009) and in healthy, hallucination prone individu-als (Brébion et al., 2010). Others have proposed that trauma-relatedintrusions – intrusive memories of previous traumatic events (Steelet al., 2005, for a theoretical model and empirical support) alsoplay an important role in clinical and non-clinical hallucinations.For example, individuals with high positive symptom schizotypy(i.e. more hallucinatory-like experiences) reported more frequenttrauma-related intrusions after watching trauma related videos orfollowing real traumatic events (Holmes and Steel, 2004; Marzillierand Steel, 2007). Empirical studies have also shown that trauma-related intrusions and flashbacks can sometimes be directly relatedto the content of AVH (e.g. Hardy et al., 2005; Scott et al., 2007),ranging from the intrusive recall of entire moments (episodes) ofprevious traumas to individual features of voices (e.g. the vocalidentity of an abuser and the emotional tone of the speaker) ofsuch events. Similarly, Andrew et al. (2008) found that traumaticlife events were reported in more than 75% of both psychotic andnon-psychotic AVH subjects, and argued that differences in thenature and interpretation of traumatic experiences differentiallyaffect beliefs about ‘voices’ in psychotic and healthy voice hearers.In sum, the frequency of intrusive memories is higher in clinicaland non-clinical hallucinators compared to controls. These intru-sive memories arise in emotionally neutral or in highly stressful(e.g. traumatic) conditions, and include both fragmentary (words,voices, emotions) and complete representations from long termmemory, in keeping with the phenomenological diversity of AVH.

2.2. Source memory and contextual integration

Intrusions are often assumed to reflect a failure of source mem-ory, which involves the ability to encode, store and retrieve specificevents in memory and bind them together with the perceptual, spa-tial, temporal and emotional context in which they occur (Johnson,2006). Individuals with schizophrenia exhibit significant deficits insource memory and contextual integration (reviewed in Hemsley,2005; Mitchell and Johnson, 2009), commonly linked to abnor-malities in hippocampal and PFC-hippocampal functioning (Boyeret al., 2007), which cannot simply be explained as an outcome ofpoor selective attention (Ferchiou et al., 2010, for supporting evi-dence). While the majority of studies have examined self\othersource discrimination (reality monitoring; e.g. Ford and Mathalon,2004) – which was excluded from the current review – a recentmeta-analysis confirms that there is no evidence for a differentialdeficit in reality monitoring in schizophrenia (Achim and Weiss,2008, for a meta-analysis). Consequently, other types of sourcememory, such as the ability to bind spatial location to remem-bered events, or recall the specific temporal sequence of eventsare also likely to be important to AVH (Larøi and Woodward, 2007,for a review). Indeed, a phenomenological study by Stephane andcolleagues showed that spatial source (i.e. location) memory isan important, separable dimension of hallucinatory experiences(Stephane et al., 2003).

Brébion et al. (2007) examined temporal context memory usinga word list learning task in a study of patients with schizophrenia,and asked participants to remember whether a word had been pre-sented in the first or the second list. Such temporal order memoryis sub-served by activity in the lateral prefrontal cortex (Jenkinsand Ranganath, 2010). Brébion et al. (2007) found that the num-ber of misattributions was higher in patients with AVH than in the

other patients. Similarly, behavioral and functional impairmentsin temporal binding have also been reported in adolescents andmature adults with psychosis, respectively (Dore et al., 2007; Weisset al., 2006), and have been linked to state and trait aspects of

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VH (Waters et al., 2006b). Steel et al. (2005) describe a theoreticalodel in which a continuum of temporal context integration ability

ccurs in the general population. They suggest that during trauma,here is a temporary reduction in the ability to integrate informa-ion within a temporal context, which leaves individuals vulnerableo traumatic intrusions. However, they also propose that healthyndividuals prone to positive symptom-like experiences have a gen-ral tendency to poorer temporal context integration. Steel et al.2005) propose that such individuals are particularly vulnerableo having memories triggered as intrusions, and that exposureo trauma in this group may have a cumulative effect – furthereakening the integration of information within the appropriate

emporal context. In contrast, three recent studies suggest thathe ability to integrate spatial location is dissimilar in individualsith psychosis (Achim and Weiss, 2008) compared to healthy indi-

iduals with AVH. For example, performance on tasks (voice andocation binding) likely to engage parahippocampal/hippocampalreas (Peters et al., 2007; Ranganath, 2010) is impaired in individ-als with schizophrenia and AVH (Chhabra et al., 2011a) but intact

n healthy hallucination-prone individuals (Badcock et al., 2008;hhabra et al., 2011b; McKague et al., submitted for publication;ee also Ruiz-Vargas et al., 1999) which suggests that at least someorms of source memory deficit may occur only in psychosis.

.3. Inhibitory control

Cognitive models of AVH have consistently focused on mecha-isms that control or limit conscious experience (e.g. Frith, 1979;ullen and Hemsley, 1987). In particular, the presence of AVH haseen linked to a reduced ability to inhibit intrusive thoughts andemories. An inhibitory mechanism is intuitively appealing since

t seems to offer a way of explaining why the sufferer does noteel s/he has direct voluntary control over the experience – a keyomponent in the definition of AVH (David, 2004). It is also neuro-ogically appealing since PFC dysfunction – the neural region largelyesponsible for inhibitory processing (Koechlin et al., 2003) – haseen consistently reported in schizophrenia (Barbalat et al., 2009;omarol-Clotet et al., 2010).

Initial studies linking cognitive inhibition and AVH in psychosisroduced inconsistent evidence (Brébion et al., 1998; Peters et al.,000). More recent research in this area has been facilitated byrawing on models of normal inhibitory processing that recognizeistinct varieties of inhibitory control (Friedman and Miyake, 2004)hich ultimately serve to prevent goal-irrelevant cognition, behav-

oral responses, and external stimuli from interrupting ongoinghoughts. For example, Harnishfeger (1995) reviewed the litera-ure and distinguished three separable dimensions of inhibitoryrocessing: (1) cognitive vs. behavioral; (2) intentional vs. uninten-ional; and (3) inhibition (the active suppression of goal-irrelevantnformation in working memory) vs. resistance to interference (gat-ng of goal-irrelevant information from entering working memory).uided by this model Waters et al. (2003) used the Hayling Sen-

ence Completion Test and the Inhibition of Currently Irrelevantemories (ICIM) task to measure intentional cognitive inhibition in

ndividuals with schizophrenia. This study demonstrated that AVHn schizophrenia are linked to a failure in intentional forms of cogni-ive inhibition. Moreover, the degree of inhibitory impairment wasignificantly correlated with the frequency of AVH. Waters et al.2003) also showed that intentional cognitive inhibition was notignificantly related to either negative, general or other positivesychotic symptoms (excluding hallucinations), suggesting a spe-ific association between intentional cognitive control and AVH.

revious studies may, therefore, have failed to find evidence of

deficit in inhibition because the tasks selected measured othere.g. unintentional) forms of inhibition. Badcock et al. (2005) lateronfirmed that the poor inhibitory control was not simply a gen-

behavioral Reviews 36 (2012) 431–438

eral feature of schizophrenia, since patients who are not currentlyhallucinating do not differ significantly in inhibition performancefrom healthy controls. In particular it was noted that the failureto suppress currently irrelevant memories was evident only asmemory traces became more strongly activated, suggesting a sub-tle interplay between intentional inhibition and episodic memoryin the genesis of AVH (Badcock et al., 2005). These findings havesince been replicated and extended by Soriano et al. (2009) usinga directed forgetting paradigm. This task measures the ability tointentionally forget recently learned information, and the resultsshowed that poor inhibitory control was significantly associatedwith the presence and frequency of AVH in schizophrenia.

Non-clinical hallucinators report a significantly higher level ofperceived control over their experiences than clinical hallucinators(Honig et al., 1998; Daalman et al., 2011). If intentional cognitiveinhibition directly underlies the subjective sense of control overhallucinations then non-clinical hallucinators might be expected todisplay intact cognitive control. Conversely, if failures of intentionalinhibition influence the objective frequency of hallucinations, assuggested by Waters et al. (2003), then healthy individuals highlypredisposed to AVH might be expected to show some impairmentof intentional inhibition compared to those with low levels ofhallucination predisposition. Paulik et al. (2007) adopted a morechallenging version of the ICIM task for use with healthy subjectsand found that individuals with high scores on the Launay SladeHallucination Scale (LSHS) exhibited subtle but consistent difficul-ties with voluntary cognitive inhibition compared to those withlow scores. Subsequent systematic examination of other formsof inhibition (Paulik et al., 2008) has confirmed that when therequirement to inhibit is unintentional no significant differencesin performance arise in healthy individuals with high and lowproneness to AVH. Together the evidence points to shared impair-ments of intentional cognitive inhibition across the continuum ofAVH. Importantly, Paulik et al. (2008) showed that poor inhibitionin non-clinical hallucinators occurred alongside intact recognitionmemory, and argued that while both groups fail to suppress, thesource of those intrusions may differ – being more closely relatedto anxiety in healthy, hallucination-predisposed individuals and toimpaired memory in patients with schizophrenia.

2.4. Lateralization and the cerebral hemispheres

The role of lateralized language (and neural) functions in theproduction of AVH remains a divided issue. In patients withschizophrenia, language processes involving both the left (Hugdahlet al., 2008a,b) and right (Sommer et al., 2008, 2010; Sommer andDiederen, 2009) hemispheres, or their disconnection (Ceccherini-Nelli et al., 2007), based on both behavioral and neuroimaging (e.g.fMRI and PET) data, have been suggested as a potential source ofAH. Increased activation of both the right (Sommer et al., 2008)and the left hemispheres (McGuire et al., 1993) has been pro-posed, but also more specifically imbalance in right hemisphereactivation has been linked to non-self origin, negative emotionalcontent or lack of conscious control of AVH. However, right- vs.left-hemisphere pathology for AVH need not be mutually exclu-sive of each other. Gainotti (1972) showed in a classic paper thatintrusive negative thoughts and emotions, what he called “catas-trophic thoughts” could be elicited from the right hemisphere afterweakening of left hemisphere inhibitory functions, due to left hemi-sphere pathology. Thus, the primary pathology may still be in theleft hemisphere, while the secondary effect of this is observed inaltered right hemisphere activation. One line of empirical data

supporting the involvement of the left temporal lobe comes fromstudies using dichotic listening (e.g. Green et al., 1994; Collinsonet al., 2009), which is a measure of left temporal lobe integrity, andin particular for speech perception. Green et al. (1994) found that

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he right ear advantage in response to dichotic presentations ofpeech sounds was reduced in both state and trait hallucinations.oreover, Collinson et al. (2009) found that patients who showed

bsence of a right ear advantage also demonstrated an accompany-ng reduction of left temporal lobe volume as measured with MRIsee also Conn and Posey, 2000). Similar conclusions can be reachedrom a study by Hoffman et al. (2007) in which trans-cranial

agnetic stimulation (TMS) applied over the left temporoparietalegion showed improvement, compared to sham-TMS, in halluci-ating patients. These findings by Hoffman et al. (2007), using TMSre also supported by evidence of a reduction of activation in theeft superior temporal gyrus, using a fMRI approach (Hugdahl et al.,008b). Thus, both direct and indirect evidence indicates that the

eft peri-Sylvian region (superior and middle temporal gyri, planumemporale, Wernicke’s area) is implicated in cognitive symptomsn schizophrenia, including AVH. In conclusion then, the evidenceuggests that lateralization of both structure and function may play

critical role in AVH, and that abnormality has been observedn both the right and left hemispheres. A disconnection view, asuggested by Ceccherini-Nelli et al. (2007) may, therefore, best fithe available empirical evidence. The conclusion of reduced lat-ralization in schizophrenia and in healthy individuals with AVHhould however be drawn with some caution since the incidencef left-handedness is elevated in both groups, which may affectateralization. For example, Sommer et al. (2010) found that there

as an incidence of 20% non-right-handers in the healthy subjectsxperiencing AVH.

Looking at the role played by the two cerebral hemispheres inon-clinical hallucinators has also provided inconsistent results,nd diverging interpretations. For example, Diederen et al. (2010)ompared three groups of subjects in an fMRI study of auditory hal-ucinations; a clinical psychotic group, non-clinical hallucinatingroup and a non-clinical, non-hallucinating group using a ver-al fluency task that would require language processing, and thusonsequently show lateralization of fMRI activation towards leftemisphere dominance. The results showed reduction of language

ateralization in the clinical hallucinating group compared to thewo other groups, caused by increased right hemisphere activationut no significant differences in lateralization of brain activationetween the two non-clinical groups, which would lend supporto a discontinuity hypothesis of auditory hallucination betweenlinical and non-clinical groups. However, the clinical hallucinat-ng group also showed increased activation in the right parietalobule, not seen in the two other groups. Since the right parietalobule repeatedly has been shown to be involved in attention reg-lation and attention focus, being central to attention networks inhe brain (Fan et al., 2005), it is possible that the difference betweenhe patients and non-patients in the Diederen et al.’s (2010) studys related more to attention factors than to hallucination factors.n support, Wang et al. (2005) reported deficits in the attentionrienting network in patients with schizophrenia.

. Discussion

In support of the continuum model, both psychotic and nonsychotic individuals with AVH experience more frequent intru-ive cognitions compared to non hallucinating controls. It must beoted that many studies use such terms as ‘intrusive thoughts’ or

intrusive memories’ interchangeably (suggesting that they war-ant clearer definition) and it is possible that these constructs areot mutually exclusive. The evidence also shows that intrusions in

oth clinical and non-clinical hallucinations are not limited to theerbatim recall of entire episodes from memory but also includehe intrusion of individual components (words, voices, emotions)f stored representations and it seems likely that this diversity of

behavioral Reviews 36 (2012) 431–438 435

intrusive cognitions underlies the phenomenological complexityof AVH. Recent functional imaging has shown that these differenttypes of vocal information are normally processed in partially dis-sociable functional pathways (see Belin et al., in press, for a reviewof clinical, psychological and neuroimaging data), which ultimatelyconverge in the MTL. Dysfunctional activation in these pathwaysmay, therefore, explain – at least in part – the shared perception ofthe reality of hallucinated voices across the continuum (Daalmanet al., 2011). We suggest that the range of intrusive cognitions inclinical and non-clinical hallucinations can also be readily inter-preted within this parallel pathways framework (Badcock, 2010,for a review) and can encompass other important phenomenolog-ical features (e.g. location in space) which characterize AVH (Plazeet al., 2011; Stephane et al., 2003).

The tendency to more frequent cognitive intrusions has alsobeen related to deficits in source memory and contextual inte-gration. Here we found only partial support for the continuitymodel. In particular, impairments in temporal context integrationhave been proposed to be associated with AVH in psychosis andin the general population. A hallmark of episodic memory is thatit contains information about the content of an event as well asthe spatial and temporal context in which it occurred. In addition,Bentall et al. (2007), in a selective review of the data, have arguedpersuasively that deficits in source memory and AVH should berelated to developmental improvements in source discriminationassociated with maturation of the frontal lobes. Thus individualdifferences in temporal context memory during childhood andadolescence might be expected to increase vulnerability to AVHeven prior to psychosis and merits considerably more empiricalinvestigation. Another aspect is that recent data has confirmedthat impaired emotion regulation, which draws heavily on frontalresources (Gyurak et al., 2009), increases both the frequency anddistress of AVH in schizophrenia (Badcock et al., 2011), it will there-fore be important for future studies to examine stress-cognitioninteractions in healthy voice hearers.

Poor inhibitory control also emerged as a common cognitivemechanism across the continuum of AVH experiences. The evi-dence suggests a specific deficit in intentional cognitive inhibition,again linked to prefrontal executive resources. The ability to inten-tionally suppress irrelevant information typically becomes moreefficient with age, usually reaching full maturity at approximately12+ years of age (Durstan et al., 2002) which coincides with theaverage age of onset of non-clinical AVH (Daalman et al., 2011).Although the average onset may be around the age of 12 years,Bartels-Velthuis et al. (2011) have shown that primary school agedchildren (7–8 years) report hearing voices, which could provideevidence for a strong trait-like factor in AVH, caused by underlyinggenetic factors. The genetics of AVH is however not an explored areaof research in the aetiology and development of hallucinated voices.It seems feasible, however, that the relatively common emergenceof hallucinations in middle childhood in the general populationmay be due (in part) to temporary immaturity or a maturationallag in inhibitory development; hence the majority of hallucinatoryexperiences are only transitory. Conversely, ongoing abnormalitiesof inhibitory control in both clinical and non-clinical hallucinatorspoint to a shared neurodevelopmental pathway consistent with a‘psychosis proneness persistence-impairment model’ of psychoticdisorder (van Os et al., 2009, for a systematic review). A gradientin severity of inhibitory control impairment (Paulik et al., 2007;Waters et al., 2003) may also contribute to the greater frequencyof hallucinations in psychosis compared to healthy voice hearers(Badcock et al., 2008; Daalman et al., 2011).

Our review also revealed a smaller but consistent thread ofevidence indicating differences in the cognitive and neural mecha-nisms linked to clinical and non-clinical AVH. Specifically, we notedtwo main differences: spatial source memory and lateralization of

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36 J.C. Badcock, K. Hugdahl / Neuroscience a

ord generation. Studies of spatial location binding in psychosisave received considerably less attention compared to reality mon-

toring (discriminating between internally and externally derivednformation). Conversely, the available evidence indicates thathe ability to integrate external sources of information (e.g. bindocation and speech) in memory is intact in healthy individualsredisposed to hallucinations and impaired in psychosis. Futureesearch is needed to understand whether spatial source memoryeficits in psychosis lead to difficulties locating ‘where’ halluci-ated voices arise, or reflect a more general difficulty in attentionalrientation to external stimulation (Arnott and Alain, in press, foreview).

The second mechanism associated with a potential discontinu-ty involved reduced lateralization in verbal fluency performancen psychotic, but not non-psychotic, AVH (Diederen et al., 2010).

ord generation typically activates the prefrontal cortex on theeft side and decreased language lateralization is well-replicated inatients with psychosis (reviewed in Li et al., 2009). The presence ofon-significant differences in lateralization of phonologically cueduency between healthy voice hearers and controls reported byiederen et al. (2010) suggests that failure to establish left hemi-

phere dominance for frontal language functions is not an essentialechanism underlying all AVH (but see Angrilli et al., 2009; Crow,

998, for discussions). Thus, it is unclear whether decreased cere-ral lateralization of language might be particularly relevant tohe distinctive features of psychotic hallucinations, such as theiregative emotional content (Sommer et al., 2008).

. Summary and main conclusions

In summary, there are many similarities in the cognitivend neural mechanisms underlying AVH in psychotic and non-sychotic groups. Indeed, Diederen et al. (2011) found in a fMRItudy several overlapping areas of activation, in 21 psychotic andon-psychotic AVH subjects, in frontal, temporal, and parietal cor-ical areas, and in the cerebellum. However, some cognitive deficitsnly occur in individuals with psychosis. We conclude that thisattern of shared and distinct cognitive mechanisms may help toxplain the phenomenological similarities and differences betweenhese groups. We agree, therefore, that a note of caution may beppropriate before accepting the continuity model of psychosisnchallenged (David, 2010). In particular, there is a potential riskhat: (a) the distinct nature of AVH in clinical and non-clinicalroups may go unassessed, and (b) the application of generic, ratherhan tailored, treatments for AVH will be ineffective, especiallyor individuals with psychosis. The review also highlights somemportant methodological issues. First, evidence against a contin-um of cognitive mechanisms for AVH may derive solely fromhenomenological differences between clinical and non-clinicalroups. Consequently, in the future, stringent testing of the con-inuum model of psychosis will require more careful matchingf both phenomenology and cognitive tasks in clinical and non-linical samples. Second, some important cognitive mechanisms ofVH may arise only in psychosis. However, the design of many cur-ent studies (e.g. comparing patients with and without AVH) ofteneads to the interpretation that only cognitive deficits specific toallucinations are relevant to understanding their aetiology. Forxample, while attentional and executive impairments are seenn relation to AVH, these are not unique or specific for AVH, butre observed across the entire spectrum of psychosis. As a conse-uence, the significance of cognitive processes that contribute to a

ange of psychotic symptoms – including AVH – may be overlooked.inally, the review was limited to only four cognitive processes, yett is clear that a range of other mechanisms are likely to play anmportant role in AVH. Most notably the role of stress and emotion-

behavioral Reviews 36 (2012) 431–438

cognition interactions may be critical in distinguishing clinical andnon-clinical AVH. We hope, therefore, that this review may help tostimulate new directions for future research.

Conflict of interest statement

The authors have no conflicts of interest to declare.

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